High plasticity in epithelial morphogenesis during insect dorsal closure.

Area of Science:

• Developmental Biology
• Evolutionary Biology
• Insect Morphology

Background:

• Insect embryos form their bodies through dorsal closure (DC), a process where epidermal flanks meet and fuse, replacing transient extraembryonic (EE) tissues.
• Drosophila melanogaster serves as a model for DC, but its reduced EE component (amnioserosa) limits broader insect comparisons.
• The red flour beetle, Tribolium castaneum, possesses complete EE tissues (amnion and serosa), offering a more representative model for studying DC evolution.

Purpose of the Study:

• To provide the first detailed, functional analysis of dorsal closure (DC) in Tribolium castaneum, an insect with complete extraembryonic (EE) tissues.
• To compare DC mechanisms in Tribolium with Drosophila, focusing on differences in the dorsal epidermis and EE tissue roles.
• To investigate the plasticity of EE tissues during DC by experimentally manipulating the serosa complement in Tribolium.

Main Methods:

• Comparative analysis of dorsal closure (DC) in Tribolium castaneum and Drosophila melanogaster.
• Detailed examination of cellular architecture and closure mechanisms in the dorsal epidermis of Tribolium.
• Experimental manipulation of EE tissue using RNA interference (RNAi) targeting Tc-zen1 in Tribolium to assess the role of the serosa.

Main Results:

• Significant differences in dorsal epidermal architecture and the final closure mechanism (zippering) were observed between Tribolium and Drosophila DC.
• The extraembryonic (EE) domain in Tribolium exhibits remarkable plasticity in morphogenetic behavior and tissue structure.
• Despite RNAi-mediated elimination of the serosa, Tribolium embryos maintained robust DC, showing conserved features and kinetics, differing substantially from Drosophila.

Conclusions:

• Insect dorsal closure (DC) mechanisms, including EE tissue behavior, are more plastic and evolutionarily adaptable than previously thought.
• The plasticity of EE tissues during DC may have facilitated the evolutionary reduction of these tissues in certain insect lineages, such as Drosophila.
• DC is essential for embryonic development, but its underlying processes demonstrate significant evolutionary flexibility, allowing for diverse EE tissue configurations across insects.